By Isabelle Hall
Rotten meat forms a significant part of the diet of numerous scavengers, including vultures and hyenas. Vultures are obligate scavengers, surviving almost solely on carrion. Instances of human consumption of rotten meat have been recorded – some reportedly practise this as a method of achieving a euphoric high, possibly through contraction of bacterial infections which reach the brain, or such an effect may be perceived following food poisoning-induced delirium. It is also thought that early humans may have procured meat through passive and confrontational scavenging (also referred to as power/aggressive scavenging, which involves chasing a predator away from its own kill), as well as through hunting (Moleón et al., 2014).
However, consumption of rotten meat generally poses significant risk to humans. After death, vertebrate microbiota levels are no longer regulated by immune homeostasis mechanisms, and they begin decomposing their host. During this process, toxic metabolites are released into the corpse, and these toxins – in addition to the bacteria themselves – can cause harm in a variety of ways. Botulism is one such issue which may arise. This potentially fatal condition is caused by the toxins released by Clostridium botulinum bacteria, which attack the nervous system and lead to impaired breathing and muscle paralysis. Carrion may contain numerous other species of bacteria which can lead to severe disease in humans, including species which contaminate the meat exogenously (contamination by pathogens in the animal’s surroundings, occurring after death). However, certain scavengers are resistant to such illnesses. Vultures are particularly adept in this regard. As they have adapted in a certain manner to utilise soaring flight and have limited agility, predation is not generally a viable method of obtaining food for them (Ruxton & Houston, 2004). Consequently, traits which enable them to survive the pathogens often found in decaying meat have been selected for over time.
One such trait is low gastric pH – the maintenance of a potent acidic environment here assists the removal of pathogens present in food. Additionally, enhanced innate immunity has been observed in vultures. This is due in part to the expression of specialised TLR1 proteins (which are present within toll-like receptor 1). Toll-like receptors are pattern recognition receptors which sense abnormal molecular features, such as those associated with pathogens. Upon recognition of such patterns, toll-like receptors can initiate signalling cascades within cells. Such activity contributes to the activation of other components of the immune system, assisting defence. Other immune adaptations identified in vultures include a modified TANK-binding kinase 1 protein. This enzyme is integral to innate immune signalling pathways, enabling induction of type 1 interferon (a group of cytokines particularly important in anti-viral defence) responses by mediating nuclear translocation of an interferon regulatory factor (Blumstein et al., 2017). One of the regions within TANK-binding kinase 1 affected by the amino acid polymorphisms identified is a ubiquitin-like domain, present on the outer surface of the protein. This region is involved in substrate phosphorylation and kinase activation; the modification thus appears to contribute to an enhanced immune system by assisting certain signalling pathways (Chung et al., 2015).
Research into the vulture gut microbiome has revealed low diversity, with two types of bacteria dominating the environment: Clostridia and Fusobacteria. The former group contains multiple bacteria which excrete toxins, and Fusobacteria includes flesh-eating species. These bacteria are also present at high levels in the gut microbiome of another carrion-eating animal – the alligator. It is not certain how these species may assist safe consumption of rotten meat, though it has been speculated that they out-compete pathogens, occupying the same niches. In this case, the vultures would act as passive hosts, having developed tolerance to the bacteria and toxins they may produce. Clostridia and Fusobacteria may also benefit vultures by degrading carrion and increasing availability of nutrients – metagenomic analysis of the turkey vulture hindgut has revealed the presence of genes for enzymes which degrade tissues, including genes associated with certain Clostridia species. This would suggest a mutualistic relationship between the bacteria and vulture, with the bacteria benefiting from a consistent supply of food (Roggenbuck et al., 2014).
The resistance to the risks of carrion-consumption demonstrated by vultures has developed through the acquisition of multiple traits, including enhanced immune defence and presence of specific gut bacteria. Further research into this field may reveal more about the evolution of obligatory scavenging, and the adaptations enabling protection against conditions which are potentially fatal in humans.
References:
Blumstein, D.T., Rangchi, T.N., Briggs, T., De Andrade, F.S. and Natterson-Horowitz, B. (2017). A Systematic Review of Carrion Eaters’ Adaptations to Avoid Sickness. Journal of Wildlife Diseases. 53 (3), 577-581. Available from: doi: 10.7589/2016-07-162
Chung, O., Jin, S., Cho, Y.S., Lim, J., Kim, H., Jho, S., Kim, H.M., Jun, J., Lee, H., Chon, A. and Ko, J. (2015). The first whole genome and transcriptome of the cinereous vulture reveals adaptation in the gastric and immune defense systems and possible convergent evolution between the Old and New World vultures. Genome Biology. 16 (1), 1-11. Available from: doi: 10.1186/s13059-015-0780-4
Moleon, M., Sanchez-Zapata, J.A., Margalida, A., Carrete, M., Owen-Smith, N. and Donazar, J.A. (2014). Humans and Scavengers: The Evolution of Interactions and Ecosystem Services. BioScience. 64 (5), 394-403. Available from: doi: 10.1093/biosci/biu034
Roggenbuck, M., Schnell, I.B., Blom, N., Bælum, J., Bertelsen, M.F., Sicheritz-Pontén, T., Sørensen, S.J., Gilbert, M.T.P., Graves, G.R. and Hansen, L.H. (2014). The microbiome of New World vultures. Nature Communications. 5 (1), 1-8. Available from: doi: 10.1038/ncomms6498
Ruxton, G.D. and Houston, D.C. (2004). Obligate vertebrate scavengers must be large soaring fliers. Journal of Theoretical Biology. 228 (3), 431-436. Available from: doi: 10.1016/j.jtbi.2004.02.005
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